Rapid proliferation and impacts of cyanobacterial mats on Galapagos rocky reefs during the 2014–2017 El Niño Southern Oscillation

Abstract

Abstract Cyanobacteria use limiting resources efficiently to take advantage of nutrient pulses, adapt to variable surroundings, and spread; this proliferation is often an indicator of ecosystem stress. We documented the sudden appearance of benthic cyanobacterial mats on a subtidal rocky reef (Roca Cousins, Galapagos Islands) during El Nino in January 2016. At this time, cyanobacteria covered 32.0% of horizontal rock surfaces and 2.6% of rock walls at 6–8\u202fm depth. Monitored photo quadrats and observations indicated that these mats were previously absent from rock walls and horizontal-sloping substrata at this site for 16\u202fyears prior to their initial appearance. The cyanobacteria was also observed at 4 other sites in the central Galapagos Islands during 2016–2018. Laboratory experiments testing the effects of temperature (28–31\u202f°C) on cyanobacterial growth and survival indicated that survival was higher at 28 than 31\u202f°C, suggesting that 31\u202f°C may be an upper thermal limit. Over two years in the field, cyanobacterial mats peaked during the warm El Nino (January 2016) and declined during two cold La Nina periods (June 2016, September 2017), ultimately declining to 6.0% cover in January 2018. Regression analysis of the temperature and cyanobacterial percent cover data indicated that temperature explained 56.9% of the variation in cyanobacteria cover in the field over the 2-year period. The cyanobacterial mats may be a consortium of several species as the closest genetic matches confirmed by Sanger sequencing (90–91.5%) were Oscillatoria spongeliae, Merismopedia glauca, and Synechococcus elongatus. Comparison of areas under the cyanobacterial mats to the adjacent uncovered rock substrata suggested that the cyanobacteria had a negative influence on underlying crustose coralline algae (CCA), as the cover of bleached CCA was 1.75 fold higher under the mats while the cover of “healthy” pink-pigmented CCA was 3 fold higher on the uncovered substrata. Short-term field experiments and feeding surveys performed to evaluate predation and to calculate electivity indices indicated that the cyanobacterial mats were avoided by dominant consumers (Eucidaris galapagensis, Pentaceraster cumingi, Nidorellia armata, and Prionurus laticlavius). Taken together, these results imply that the novel appearance of cyanobacterial mats in the Galapagos rocky subtidal zone was facilitated by unusually warm temperatures during the 2014–2017 El Nino (28–29\u202f°C) and that the cyanobacteria were regulated by temperature, but not by consumers. Future outbreaks of mat-forming cyanobacteria during El Nino periods may negatively impact the abundance of CCA and have direct and indirect negative effects on other components of marine benthic communities that rely on CCA as either a settlement substratum or food source.